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Microbiome Composition Within a Sympatric Species Complex of Intertidal Isopods (Jaera Albifrons)

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Microbiome Composition Within a Sympatric Species Complex of Intertidal Isopods (Jaera Albifrons) RESEARCH ARTICLE Microbiome composition within a sympatric species complex of intertidal isopods (Jaera albifrons) Marius A. Wenzel*, Alex Douglas, Stuart B. Piertney School of Biological Sciences, University of Aberdeen, Aberdeen, United Kingdom * [email protected] a1111111111 a1111111111 a1111111111 Abstract a1111111111 a1111111111 The increasingly recognised effects of microbiomes on the eco-evolutionary dynamics of their hosts are promoting a view of the ªhologenomeº as an integral host-symbiont evolution- ary entity. For example, sex-ratio distorting reproductive parasites such as Wolbachia are well-studied pivotal drivers of invertebrate reproductive processes, and more recent work is OPEN ACCESS highlighting novel effects of microbiome assemblages on host mating behaviour and devel- Citation: Wenzel MA, Douglas A, Piertney SB opmental incompatibilities that underpin or reinforce reproductive isolation processes. How- (2018) Microbiome composition within a ever, examining the hologenome and its eco-evolutionary effects in natural populations is sympatric species complex of intertidal isopods challenging because microbiome composition is considerably influenced by environmental (Jaera albifrons). PLoS ONE 13(8): e0202212. https://doi.org/10.1371/journal.pone.0202212 factors. Here we illustrate these challenges in a sympatric species complex of intertidal isopods (Jaera albifrons spp.) with pervasive sex-ratio distortion and ecological and beha- Editor: Cheryl S. Rosenfeld, University of Missouri Columbia, UNITED STATES vioural reproductive isolation mechanisms. We deep-sequence the bacterial 16S rRNA gene among males and females collected in spring and summer from two coasts in north- Received: February 20, 2018 east Scotland, and examine microbiome composition with a particular focus on reproductive Accepted: July 29, 2018 parasites. Microbiomes of all species were diverse (overall 3,317 unique sequences among Published: August 29, 2018 3.8 million reads) and comprised mainly Proteobacteria and Bacteroidetes taxa typical of Copyright: © 2018 Wenzel et al. This is an open the marine intertidal zone, in particular Vibrio spp. However, we found little evidence of the access article distributed under the terms of the reproductive parasites Wolbachia, Rickettsia, Spiroplasma and Cardinium, suggesting alter- Creative Commons Attribution License, which native causes of sex-ratio distortion. Notwithstanding, a significant proportion of the vari- permits unrestricted use, distribution, and reproduction in any medium, provided the original ance in microbiome composition among samples was explained by sex (14.1 %), nested author and source are credited. within geographic (26.9 %) and seasonal (39.6 %) variance components. The functional rel- Data Availability Statement: Raw sequence data evance of this sex signal was difficult to ascertain given the absence of reproductive para- alongside all relevant metadata are deposited in the sites, the ephemeral nature of the species assemblages and substantial environmental NCBI short-read archive (SRA) at accession variability. These results establish the Jaera albifrons species complex as an intriguing sys- SRP132549. tem for examining the effects of microbiomes on reproductive processes and speciation, Funding: This work was funded by the UK Natural and highlight the difficulties associated with snapshot assays of microbiome composition in Environment Research Council (NERC), grant NE/ M015661/1, awarded to SBP and AD. The funders dynamic and complex environments. had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. PLOS ONE | https://doi.org/10.1371/journal.pone.0202212 August 29, 2018 1 / 19 Microbiome composition in Jaera albifrons spp. Introduction Microbiomes have long been recognised as important functional extensions of their host's physiological and broader ecological phenotype. For example, microbiomes affect fundamen- tal physiological processes associated with digestion, immune system function, disease aetiol- ogy and behaviour [1±3], ecological processes such as nutrient cycling at the plant-root/soil interface [4, 5] and calcification, proliferation and community structure of coral reefs [6, 7], as well as key evolutionary transitions such as the origin of mitochondria [8], gain of photosyn- thetic function in eukaryotic cells [9] or the parallel and convergent evolution of biolumines- cent ªlight organsº in squid and angler fishes [10, 11]. From an evolutionary perspective, microbiome composition is also implicated in reproductive isolation and speciation via affect- ing chemosensory cues essential for mating preference [12] or causing fundamental develop- mental incompatibilities and hybrid breakdown [13]. These insights have given rise to the ªhologenomeº concept of considering the host macro-organism and its associated microbiome as an integral evolutionary entity [14±16]. As such, studying the multi-layered effects of host- microbiome interactions holds immense value for a broad array of pure and applied disci- plines ranging from medicine and agriculture to molecular physiology and ecosystem ecology and evolution [14, 17, 18]. A centrally important phenomenon that underlines how microbiomes may affect eco-evo- lutionary processes in their hosts is sex-ratio distortion in invertebrates caused by infection with cytoplasmic reproductive endoparasites. Wolbachia, Rickettsia, Spiroplasma, Cardinium bacteria and Microsporidian fungi infect the reproductive organs of many arthropod and nematode species and are cytoplasmically transmitted from mother to offspring [19±23]. As a means of promoting transmission and infection prevalence in the population, these parasites manipulate host reproductive biology to distort host sex-ratios in favour of infected females by induction of parthenogenesis, feminization of male offspring, killing of male embryos, disrup- tion of sex-chromosome inheritance, or cytoplasmic incompatibility between individuals with different infection statuses [19, 22, 24]. This demographic disruption can lead to erosion of genetic diversity and phylogenetic signal akin to a bottleneck or selective sweep since most of the population will eventually be descended from few infected matrilines [25, 26]. Con- versely, Wolbachia infection can also promote diversification via horizontal gene transfer to the host [22], and initiation or reinforcement of reproductive isolation and speciation through cytoplasmic incompatibility between populations with mixed infections [27, 28]. Not least, Wolbachia infection can perturb overall microbiome composition, often in sex-specific fashion with downstream physiological effects [29±32]. In concert, these factors firmly establish Wol- bachia and other reproductive parasites as pivotal agents in driving the evolution of many invertebrates. Beyond the obvious value in studying prominently important taxa such as Wolbachia and other reproductive parasites, key to gaining a proper understanding of the effects of the holo- genome on any facet of eco-evolutionary dynamics is the capacity to examine microbiome- wide patterns of diversity in free-living non-model systems. The wide availability of high- throughput DNA sequencing has enabled rapid characterisation of microbial species composi- tion in virtually any type of field sample, and is poised to revolutionise our understanding of how the hologenome operates and evolves in the wild [33, 34]. However, a pre-requisite to thoroughly understanding microbiome composition is an appreciation of potential environ- mental sources of variation. Abiotic factors in dynamic natural environments may confer considerable spatio-temporal variation in ephemeral uptake and proliferation of commensal microbionts that may not necessarily be functionally linked to host metabolism. For example, microbiome composition in marine copepods is contingent on seasonal and spatial differences PLOS ONE | https://doi.org/10.1371/journal.pone.0202212 August 29, 2018 2 / 19 Microbiome composition in Jaera albifrons spp. in water temperatures [35], and littoral Hymeniacidon heliophila sponges can display small- scale variation in microbiome composition between subtidal and intertidal specimens [36]. Conversely, the microbiomes of various marine nematode species are not obviously structured across habitats even on a global scale [37]. These examples highlight the need for an initial assessment of the degree of environmental variation in microbiomes before attempts are made to identify functionally relevant variation in the hologenome and its contribution to host ecol- ogy and evolution [38]. The Jaera albifrons (sensu lato) species complex of sympatric intertidal isopods is an intui- tively attractive study system for examining the links between reproductive parasites, micro- biomes and host eco-evolutionary processes. In Europe, the complex comprises Jaera albifrons sensu stricto, Jaera ischiosetosa, Jaera praehirsuta and Jaera forsmani, with Jaera nordmanni as a congeneric outgroup taxon [39±41]. All species are common across North Atlantic coasts and often form mixed populations in sympatry or parapatry along the intertidal zone. The ingroup species are reproductively isolated through female preference for tactile courtship stimuli administered by males [41, 42], genetic incompatibilities conferring rapid hybrid breakdown [41, 42], and ecological zonation due to species-specific
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